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PASTOS 2012. ISSN: 0210-1270 PASTOS, 42 (2), 137 - 160 137

FLORA OF THE IN THE CHILEAN ESPINALES: EVIDENCE OF COLONISATION

I. MARTÍN-FORÉS1, M. A. CASADO1*, I. CASTRO2, C. OVALLE3, A. DEL POZO4, B. ACOSTA-GALLO1, L. SÁNCHEZ-JARDÓN1 AND J. M. DE MIGUEL1

1Departamento de Ecología. Facultad de Biología. Universidad Complutense de Madrid. Madrid (España). 2Departamento

de Ecología. Facultad de Ciencias. Universidad Autónoma de Madrid. Madrid (España). 3Instituto de Investigaciones

Agropecuarias INIA-La Cruz. La Cruz (). 4Facultad de Ciencias Agrarias. Universidad de Talca. Talca (Chile).

*Author for correspondence: M.A. Casado ([email protected]).

SUMMARY

In Chile’s Mediterranean , over 18% of plant are alien. This is particularly noteworthy in some agrosilvopastoral systems such as the espinales, which are functionally very similar to the Spanish dehesas and are of great ecological and socioeconomic interest. In the present paper we analyse Chile’s non-native flora, considering three scales of analysis: national, regional (the central region, presenting a Mediterranean ) and at community level (the espinales within the central region). We compare this flora with that recorded in areas of the with similar lithological and geomorphological characteristics, and land use. We discuss possible mechanisms that might have been operating in the floristic colonisation from the Mediterranean Basin to Chile’s Mediterranean region.

Key words: Alien plants, , Chile, life cycle, .

INTRODUCTION

Historically, the transit of goods, domestic animals and people has favoured the flow of wild organisms around the planet (Lodge et al., 2006), a fact that is often associated with the introduction of cultural systems, which have contributed to generating new environmental and socioeconomic scenarios (Le Houérou, 1981; Hobbs, 1998; Grenon and Batisse, 1989). The current globalisation process is increasing landscape changes and ecosystem disruptions by disturbance and therefore facilitating

Bases de datos: http://polired.upm.es/index.php/pastos (España), AGRIS (Italia), CAB Abstracts (Reino Unido), CABI Full Text (Reino Unido), Catálogo LATINDEX (México), DIALNET (España), ICYT Ciencia y Tecnología (España) 138 PASTOS, 42 (2), 137 - 160 PASTOS 2012. ISSN: 0210-1270 Martín-Forés et al. Plant species colonization in Chilean espinales the transit of organisms (Paskoff and Manríquez, 1999; Rouget et al., 2003; Dukes and Monney, 2004; Schwartz et al., 2006). These ‘assisted dispersals’ enable species to cross biogeographical boundaries that have previously limited their distributions. Species that have been transported from one region to another are defined as alien or exotic to that newly occupied region (Richardson et al., 2000). Most of these species fail to establish self-perpetuating populations, but some of them do succeed and become naturalized (Sax and Brown, 2000). Regardless of the factors enabling establishment, the main consequence of this naturalisation is that alien species significantly contribute to the global floristic (taxonomic and phylogenetic) homogenization of regional floras ( et al., 2009). Despite the fact that introduction of species increases diversity at short temporal and small spatial scales, in the medium and long term, interactions with native species can lead to extinctions (Pyšek and Richardson, 2006). The net effect will depend upon the spatial and temporal scales considered and on the balance between naturalisations and extinctions (Sax et al., 2002). Nonetheless, the resulting ecological consequence is the coexistence of native species with exotic ones, quite often in the same community. The origin and composition of these novel communities are of great interest to understand their functioning and possible management.

Transcontinental naturalisation in Chile’s flora

Mediterranean-type ecosystems around the offer a great chance to compare and understand the mechanisms determining the success of species introduced into a given region (Kruger et al., 1989; Groves and Di Castri, 1991). The different presenting a have had different environmental histories associated with the density of human populations as well as the time and intensity of the changes that people have caused in the territory. In the Mediterranean Basin, anthropic modification of the landscape is millenary; however, rates of species extinction and naturalisation are low in comparison with other Mediterranean regions (Greuter, 1994). This fact is explained as a process of co-evolution of plants with people (Di Castri, 1981). Conversely, other Mediterranean areas have undergone a rapid change following successive cultural colonisations, some of these relatively recent, a fact that accounts for the current ecological conditions threatening the of these areas (Underwood et al., 2009). As with other Mediterranean regions, Chile is recognised as a (Ormazabal, 1993), with high levels of regional and national , possibly related with its biogeographic isolation (Myers et al., 2000). Its flora comprises 5364 native taxa, including species and subspecies (Marticorena and Quezada, 1985; Marticorena and Rodriguez, 1995, 2001) and between 552 and 723 alien species, depending on the PASTOS 2012. ISSN: 0210-1270 PASTOS, 42 (2), 137 - 160 139 Martín-Forés et al. Plant species colonization in Chilean espinales author considered (Arroyo et al., 2000; Castro and Jaksic, 2008). Paradoxically, despite the large amount of alien species present and their early colonisation, Chile has been considered a region that has been less invaded or is in an earlier stage of invasion than other Mediterranean regions of the world (Arroyo et al., 2000; Figueroa et al., 2004; Castro and Jaksic, 2008). The arrival of exotic species to Chile started with the European colonisation in the XVI century (Arroyo et al., 2000; Figueroa et al., 2004), which marked the first deliberate introduction of animals and plants ( et al., 1991; Jaksic, 1998). The rate of species entry in these early days is unknown, since the initial systematic botanic descriptions of flora date from the XVIII century and were performed by botanists who were more interested in describing the native species than the exotic ones (Gay, 1845-1854; Reiche, 1896-1911). By the end of the XVIII century, numerous exotic species had become naturalised in Chile (Figueroa et al., 2004), such as Cardamine hirsuta L., Medicago polymorpha L., Spartium junceum L. and Bromus hordeaceus L. (Castro et al., 2005). Although this species introduction has not been consistent over time, a rate of two to three species per year is estimated, which is lower than the four to six species recorded for other Mediterranean regions (Groves, 1991; Kloot, 1991, Rejmánek et al., 1991; et al., 2003).

Processes and mechanisms in species introduction

Changes in land use constitute the main factor determining processes of colonisation and naturalisation of plant species (Le Houérou, 1991; Huston, 1994; Holmgrem et al., 2000). Among the most influential factors, deforestation, fires and particularly agricultural practices have been highlighted (Le Houérou, 1991; Cowling et al., 1996; Williamson, 1996; Hobbs, 1998). With regard to deforestation, although Chile still has one of the biggest areas of temperate in (Donoso, 1993), much of it has been deforested for pastures or croplands. This process started in the XVI century, although the main boom was during the middle of the XX century, with the expansion and intensification of crops (Echeverría et al., 2006) and the spread of forestry plantations. In relation to fire, unlike other Mediterranean climate areas, fire has not constituted a factor of natural disturbance in Chile (Muñoz and Fuentes, 1989; Gómez- González and Cavieres, 2009), a fact that accounts of the absence of specific adaptations in native species. Although there is evidence of fires of human origin in earliest settlements in the region, around 14 000 years ago, these were not significant until the arrival of the Spanish (Aronson et al., 1998; Aravena et al., 2003; Villa-Martínez et al., 2003). Subsequently, fires became more frequent and intense, and currently about 5000 ha of native scrubland are burnt each year, the vast majority of these fires being 140 PASTOS, 42 (2), 137 - 160 PASTOS 2012. ISSN: 0210-1270 Martín-Forés et al. Plant species colonization in Chilean espinales intentional (Gómez-González and Cavieres, 2009). It has been suggested that plant communities under novel fire regimes are more susceptible to invasion than those under a natural (historical) fire regime (Trabaud, 1991; D’Antonio, 2000). However, different studies that have analysed the effects of fire upon native and non-native Chilean flora appear to indicate that fire is not a relevant factor with regard to favouring non-native species (Keeley and Johnson, 1977; Holmgrem et al. 2000; Gómez-González et al., 2010). Fire does, however, constitute a notable advantage for the establishment of annual plants, which are poorly represented in Chile’s native flora (Arroyo et al., 1995). The implementation of European agricultural culture in the XVI century leaded to big changes in land uses and landscapes in Chile, the extent of which are yet not well known (Turner et al., 1995). The effects of agriculture have been both direct (ploughing, cropping and grazing) and indirect (fire and deforestation, employed as techniques for preparing the land for agriculture and livestock farming). Livestock was introduced into Chile, perhaps at the same time as the colonisation by Europeans. Other herbivores, however, such as rabbits and hares, were brought more recently, in the XIX century (Jaksic and Soriger, 1981). Several studies have associated the naturalisation of exotic plant species with grazing by both livestock (Holmgren et al., 2000; Pauchard and Alaback, 2004; Del Pozo et al., 2006; HilleRisLambers et al., 2010) and rabbits (Sáiz and Ojeda, 1988; Holmgren et al., 2000; Holmgren, 2002). The effect of grazing on native or non-native species has been characterised using morphofunctional plant traits, revealing differences in their response. For instance, grazing appears to favour some exotic creeping species, such as Erodium cicutarium (L.) L’Hér. and some leguminous species, in detriment to the upright ones, the latter more closely associated with native species (Holmgren et al., 2000). Grazing also favours substitution of native hemicryptophytes by both native and non-native annuals, capable of resisting periods of drought stress as seeds. Many exotic plants were also introduced associated with crops, and became widely distributed as a result of the importance of agriculture in the country (Castro et al., 2005). Crop fields, particularly along their succession stages following abandonment, constitute the ecosystems presenting the highest values for richness and cover of non-native plants in Chile (Figueroa et al., 2011). Since colonisation the introduction process has continued, although with different rates along time. Thus, Aronson et al. (1998) highlight an initial wave of exotic species from 1880 to 1920 associated with transformation of the landscape. Fuentes et al. (2008) recognise an initial phase (1910- 1940) associated with intense development of agriculture (Cariola and Sunkel, 1982), as well as a second phase (1980-2000) related with a sharp increase in the mechanisation of farms and forest plantations at large scale. Matthei (1995) describes a sustained increase PASTOS 2012. ISSN: 0210-1270 PASTOS, 42 (2), 137 - 160 141 Martín-Forés et al. Plant species colonization in Chilean espinales in the naturalisation of exotic species from 1894 to 1934 associated with wheat imported from other countries. Although many species were accidentally introduced into Chile (Arroyo et al., 2000), many were taken for agricultural, medicinal, culinary and, more recently, ornamental purposes. Since the arrival of the Spanish, species were introduced associated with hay for livestock fodder and with wool and cereals. Endozoochory likely constitutes the most frequent mechanism of effective seed dispersal. However, during transit from Spain to Chile, exozoochory was probably the most effective means of dispersal, given the difference in time between the transoceanic voyage and the time required for seeds to pass through an animal’s digestive tract (generally less than 1 week; Malo and Suárez, 1997). was not the only centre of introduction of non-native species to Chile. During the Gold Rush, in the middle of the XIX century, there was intense wheat trading with (Davis, 1894), a fact which mobilised other species, together with grain and straw, in both directions (Le Houérou, 1991; Jiménez et al., 2008), especially from Chile to California.

Comparative studies of transcontinental naturalisation

Comparison of non-native floras between climatically similar regions constitutes a very useful tool for understanding aspects associated with the species naturalisation process (Pauchard et al., 2004, Hierro et al., 2005). It can help us to understand the effects of changes in the landscape associated with historical or cultural scenarios upon the naturalisation process (Kruger et al., 1989; Aschman, 1991). Among comparative studies of different regions with Mediterranean , those between Chile and California have been intensely analysed (e.g. Parsons, 1976; Arroyo et al., 1995; Holmgren et al., 2000; Pauchard et al., 2004; Jiménez et al., 2008). These researches highlight the large number of species common to both regions (386, which is 64% of Chile’s non-native flora; Pauchardet al., 2004), as well as the fact that their communities are undergoing different process of invasion with similar consequences of floristic homogenization (Figueroa et al., 2011). However, to date there have been no comparative studies between Chile and Spain, despite their climatic and geomorphological similarity, the historical relationships that favoured the entry of species into Chile and the large number of species common to both countries. Many of these naturalised species are associated with the espinal, an agroecosystem presenting a management system and structure similar to those of the Spanish dehesa (Ovalle and Avendaño, 1987; Ovalle et al., 1990). However, as these agricultural systems are similar in both countries, we are not fully aware of the mechanisms underlying the arrival of determined species and the subsequent naturalisation and spread thereof. 142 PASTOS, 42 (2), 137 - 160 PASTOS 2012. ISSN: 0210-1270 Martín-Forés et al. Plant species colonization in Chilean espinales

The aim of this paper is to analyse the relative significance of the biogeographic origin, lifecycle and representativeness of taxonomic families in Chile’s non-native flora. We considered three scales of analysis: national, regional (the central zone presenting a Mediterranean climate) and community (the espinales within the central zones). In the third case, we also conducted a comparative study with Mediterranean from the Iberian Peninsula in order to identify the degree of similarity in the floristic composition of communities with comparable ecological and agronomic characteristics.

MATERIAL AND METHODS

Study area

The espinal is an anthropic savannoid formation characterised by dispersed trees of Acacia caven Mol. (the espino) within an herbaceous matrix comprising mainly annual plants of Mediterranean origin (Olivares and Gastó, 1971; Ovalle et al., 2005; del Pozo et al., 2006). It supports a rural population of approximately 350 000 people, as well as the largest Chilean livestock: 800 000 and 250 000 cows. It covers an area of two million hectares in Chile’s central zone, ranging along the Central Valley and the western slopes of the Coastal mountain range (Ovalle et al., 1999). It currently occupies mainly the dryland sectors (Figure 1), from the river Petorca (32° S), bordering on the arid Mediterranean region, to the river Laja (37º S), bordering on the perhumid region (Fuenzalida and Pisano, 1965; Di Castri, 1968; Quintanilla, 1981; Rodríguez et al., 1983). Further north, in the arid and perarid regions, some espinales can be found, preferentially located in valley bottoms (Follman and Matte, 1963; Rodríguez et al., 1983). Their distribution is associated with Mediterranean-climate areas, albeit with very variable annual rainfall, from 160-200 mm at its northern limit and up to 1000- 1200 mm at the southern one. It presents high species diversity (Gulmon, 1977; Solbrig et al., 2002; Del Pozo et al., 2002) and to date, 215 species have been identified only in the Cauquenes region (Ovalle et al., 1987). It originated through changes in land uses after the Spanish conquest; the native sclerophyllous forest was cleared in order to open up land for agriculture and livestock farming, which favoured gradual invasion by the exotic species A. caven (Gulmon, 1977; Armesto and Pickett, 1985; Ovalle et al., 1990), possibly from South America’s (Holmgren, 2002). The espinal is an agrosilvopastoral system presenting much similarity with the Spanish dehesas and Portuguese montados. It has traditionally been based upon two models of management: continuous extensive grazing in flatlands, occasionally inundated during winter, and rotation of grazing and cereal cropping in the better drained hillsides (Ovalle et al., 2005). In the latter case, the espino is periodically cut PASTOS 2012. ISSN: 0210-1270 PASTOS, 42 (2), 137 - 160 143 Martín-Forés et al. Plant species colonization in Chilean espinales down for firewood and charcoal. The land is subsequently ploughed for sowing cereal crops. After one or two years’ harvest, depending upon the fertility of the soil, the land is abandoned and colonised by herbaceous species, while shoots grow from the stump of the espino. In this phase, the land is used for extensive grazing with a low stocking rate of approximately one sheep/ha (Del Pozo et al., 2006). The grazing period prior to the following cropping cycle is variable, from three to 40 years, depending on the fertility of the soil.

FIGURE 1 Location of Chile (in grey) in South America and enlargement of the Central zone. The shaded area represents the main distribution areas of espinal (modified from Ovalle et al., 1999). Localización de Chile (en gris) dentro de Sudamérica y ampliación de la Zona Central. La región sombreada representa el área de distribución de los espinales (modificado de Ovalle et al., 1999). 144 PASTOS, 42 (2), 137 - 160 PASTOS 2012. ISSN: 0210-1270 Martín-Forés et al. Plant species colonization in Chilean espinales

The espinal is currently more degraded than in past times. In the first place, an increasingly greater area of the espinales in the Central Valley is being replaced by intensive irrigation agriculture. Furthermore, many owners have abandoned their traditional farming activities for forest plantations (approximately 80 000 ha/year), mainly of Pinus radiata D. Don or globulus Labill. Finally, the territory still maintaining functional espinales has usually low fertility and soil erosion, leading to low agricultural production. At present, 40% of the area is occupied by espinales with very little tree cover (<25%) and 4% is dominated by romerillo (Baccharis linearis (Ruiz and Pav.) Pers.), which indicates a situation of degradation and abandonment. Under these circumstances, the cereal-pasture rotation system is in decline and limited to small areas, almost exclusively for people’s own consumption.

Methodology

For our research we developed a database containing all non-native species found in Chile. We used the catalogue of Chilean flora by Marticorena and Quezada (1985, 1987), along with information provided by the Laboratorio de Invasiones Biológicas de la Universidad de Concepción (http://www.lib.udec.cl/database.html). This list was complemented with an extensive bibliographic revision incorporating some exotic species recently cited in the country. Each species was characterised by assigning its taxonomic family, area of origin, life cycle and distribution range within Chile. To assign the area of origin and life cycle we used different regional floras, fundamentally Flora Iberica (Castroviejo et al., 1986-2010), Flora Europaea (Tutin et al., 1964-80) and Flora del Cono Sur (Zuloaga et al., 2008). As regions of origin we considered the four big : , , America and Australasia. Apart from these four large regions we considered independently the Mediterranean Basin (SE, S and SW of Europe, N Africa and SW ), given the non-native typology of species present in Chile. Species present in more than one were classified as Cosmopolitan. As for the life cycle trait, we classified them into three groups: annual, perennial herbaceous and woody species. Finally, for the distribution range within Chile we took the 15 administrative regions as units (from the Tarapacá Region in the to the Magallanes Region at the southern limit), excluding the species present only on the islands belonging to Chile ( and the Juan Fernández archipelago). We obtained these data mainly from Castro et al. (2005), Martincorena (http://www.lib.udec.cl/database.html) and Zuloaga et al. (2008). We considered the set of non-native species present throughout the country, as well as those distributed only in the central zone (from the Coquimbo region in the north to the Bío-Bío Region in the south; Figure 1). PASTOS 2012. ISSN: 0210-1270 PASTOS, 42 (2), 137 - 160 145 Martín-Forés et al. Plant species colonization in Chilean espinales

In order to complement our database of non-native species, in 2010 we conducted field samplings, both in Chilean espinales and in Spanish Mediterranean grasslands. In each country we selected 15 sites and in each one we chose two 10 x 10 m plots in which we randomly distributed six 50 x 50 cm quadrants. In each quadrant we recorded the presence of all plant species. Each species was assigned a value of frequency according to the number of sites in which it was recorded in each country. The 30 sites selected presented similar lithological characteristics (acidic materials associated with igneous or metamorphic rocks), geomorphological ones (undulating topography) and those relating to use history (management for extensive livestock farming). In the case of Chile the 15 sites were distributed within the Mediterranean region, over more than 600 km, from 32º 31’ 35’’ to 37º 00’ 10’’ S latitude. In the case of Spain the 15 sites were distributed within the centre-western areas (Extremadura, N Andalucía and W Castilla- La Mancha, from 40º 14’ 45’’ to 37º 51’ 40’’ N latitude). For all species of European origin, we standardised the nomenclature in accordance with Flora Iberica (Castroviejo et al., 1986-2010), and in the case of families as yet unpublished in this study, with Flora Europaea (Tutin et al., 1964-80).

RESULTS

The list of Chile’s non-native flora comprises 773 species or subspecies, which, following exclusion of spurious citations, was reduced to 698 taxa (548 in the central zone and 75 in the espinales), 50 of which are woody species and the rest herbaceous ones. This large set of species is distributed into 72 families, of which the best represented ones at country scale are (19.8% of species), (13.9%) and Fabaceae (10.2%). This distribution of species into families is very similar when the Chile’s central zone was exclusively considered (Figure 2). However, the spectrum of families present in the flora of the espinales is very different, and is characterised by a higher proportion of Poaceae, Caryophylaceae, Rubiaceae, Rosaceae and Geraniaceae, and a decrease in the proportion of . This distribution into families of the espinales is relatively similar to that seen in Spanish grasslands, except for the fact that Spain presents more Fabaceae (18.5% vs 12%) and Brassicaceae (3.5% vs 1.3%), and the espinales more Caryophylaceae (9.3% vs 7.1%), Rubiaceae (4% vs 1.3%), Rosaceae (5.3 vs 1.3%) and Geraniaceae (5.3% vs 1.8%). 146 PASTOS, 42 (2), 137 - 160 PASTOS 2012. ISSN: 0210-1270 Martín-Forés et al. Plant species colonization in Chilean espinales

Each histogram shows the frequency calculated at country scale (white bars; n = 698 species), of Chile’s central zone (light grey bars; n = 547 species) and of the espinales (dark grey bars; n = 75 species). In the case of Spanish grasslands (black bars) frequency was calculated with the total number of species found in the field samplings (n = 229 species)

FIGURE 2 Frequency histograms of the distribution of non-native species according to taxonomic families. Only the nine most represented families are shown. Histogramas de frecuencia de la distribución de las especies no nativas según la familia a la que pertenecen. Solo se muestran las nueve familias mejor representadas. PASTOS 2012. ISSN: 0210-1270 PASTOS, 42 (2), 137 - 160 147 Martín-Forés et al. Plant species colonization in Chilean espinales

With regard to the area of origin of Chile’s non-native species, at the scale both of country and of the central zone, species of Eurasian origin (39.7%) dominate and, to a lesser degree, those of Mediterranean origin (28.4%) (Figure 3). However, when only the flora of theespinales is considered, the species from the Mediterranean Basin increase to 49.3% and those of Eurasian origin to 48%, thus Eurasia in the broader sense constitutes the area of origin of 97.3% of non-native species. This tendency is maintained in Spanish grasslands, with values of 97.8% for species from Eurasia (72.1 and 25.7% for species of Mediterranean and Eurasian origin, respectively).

Each histogram shows the frequency calculated at country scale (white bars; n = 698 species), of Chile’s central zone (light grey bars; n = 547 species) and of the espinales (dark grey bars; n = 75 species). In the case of Spanish grasslands (black bars) frequency was calculated with the total number of species found in the field samplings (n = 229 species).

FIGURE 3 Frequency histograms of the distribution of non-native species according to region of origin. Histogramas de frecuencia de la distribución de las especies no nativas según la región biogeográfica de origen. 148 PASTOS, 42 (2), 137 - 160 PASTOS 2012. ISSN: 0210-1270 Martín-Forés et al. Plant species colonization in Chilean espinales

Both in Chile as a whole and in the central zone, the vast majority of non-native species are herbaceous, both annual (55.8%) and perennial (37%) (Figure 4). This trend is accentuated in the espinales, where none exotic woody species have been found and annual plants represent 84%, a value very similar to the 81.2% of annual species found in Spanish grasslands. Life cycle (annual, herbaceous perennial and woody) is not independent from the area of origin of the non-native species (table of contingency between areas of origin x life cycle, c2 = 169.18, p < 0.001): among the species of African and American origin there are significantly more woody and perennial herbaceous plants than expected at random; among those of Mediterranean origin there are significantly more annual species; and among those of Australian origin there are significantly more woody species.

For Chile, the central zone and the espinal we only considered non-native species. For Spanish grasslands, we calculated frequency with the total number of species found in the field samplings.

FIGURE 4 Frequency histograms of the distribution of non-native species according to their life cycle: annual (black bars), perennial herbaceous (grey bars) and woody (white bars) plant. Histogramas de frecuencia de la distribución de las especies no nativas según su forma biológica: anual (barras negras), herbácea perenne (barras grises) y leñosa (barras blancas).

In the field samplings we recorded a total of 229 species in the Spanish grasslands and 152 in the Chilean espinales, 49% of which were non-native. Of the 10 most common species in Spain, all but one (Agrostis pourreti Willd) can be found in the catalogue of non-native species of Chile; moreover, they were found in the sampling in the espinales (Table 1). Likewise, of the 10 most common species in the espinales, all but one (Soliva sessilis Ruiz and Pav.) are non-native and have been found in sampling conducted in Spain. PASTOS 2012. ISSN: 0210-1270 PASTOS, 42 (2), 137 - 160 149 Martín-Forés et al. Plant species colonization in Chilean espinales

TABLE 1 List of the 10 most frequent species in Spain (a) and in Chile (b). For each species taxonomic family, distribution in Spain and Chile and frequency of appearance in each country are shown. Listado de las 10 especies más frecuentes en España (a) y Chile (b). Para cada especie se indica la familia taxonómica, su distribución española o chilena y la frecuencia de aparición en cada país.

Frequency in Frequency in Species Family Distribution Spain (%) Chile (%) a) Spain Plantago lanceolata Plantaginaceae Both 42.2 11.4 Bromus hordeaceus Gramineae Both 42.8 63.6 Trifolium campestre Leguminosae Both 49.7 1.9 Vulpia muralis Gramineae Both 50.3 22.2 Hypochoeris glabra Compositae Both 50. 6 61. 7 Plantago coronopus Plantaginaceae Both 56.9 0.1 Agrostis pourretii Gramineae Spain 58. 9 0.0 Trifolium glomeratum Leguminosae Both 58. 9 23.1 Tolpis barbata Compositae Both 63.1 5.3 Leontodon taraxacoides subsp. Compositae Both 69.4 83.3 longirostris b) Chile Petrorhagia prolifera Caryophyllaceae Both 6.4 33.6 Soliva sessilis Compositae Chile 0.0 33. 9 Erodium cicutarium Geraniaceae Both 15.8 34.7 Trifolium dubium Leguminosae Both 8.3 35.0 Briza minor Gramineae Both 4.2 46. 7 Erodium botrys Geraniaceae Both 3.3 49.7 Hypochoeris glabra Compositae Both 50. 6 61. 7 Bromus hordeaceus Gramineae Both 42.8 63.6 Aira caryophyllea Gramineae Both 8.8 64.4 Leontodon taraxacoides subsp. Compositae Both 69.4 83.3 longirostris

DISCUSSION

Arroyo et al. (2000) and Figueroa et al. (2004) consider that in continental Chile there is a total of 707 naturalised non-native species and subspecies. This value is somewhat higher than the 698 taxa considered in this paper, approximately 12% of the total flora. Despite the fact that some recent introductions have been done, a greater amount of 150 PASTOS, 42 (2), 137 - 160 PASTOS 2012. ISSN: 0210-1270 Martín-Forés et al. Plant species colonization in Chilean espinales species have been excluded from the list due to being spurious citations. The amount of exotic species in Chile, however, is likely higher, considering the little botanical prospection conducted in certain parts of the country. Thus, during the sampling and in view of the lack of confirmation, at least 5 species had not been previously cited: Aphanes microcarpa (Boiss. and Reut.) Rothm., Logfia minima (Sm.) Dumort., erecta (L.) G. Gaertn., B. Mey. and Scherb., Trifolium cernuum Brot. and Vulpia ciliata Dumort. Considering only the central Mediterranean zone, Figueroa et al. (2011) recognised 2395 native species and 507 non-native ones, which account for 18% of the flora in this region (Arroyo and Cavieres, 1997; Arroyo et al., 2000). In this case, our data contain 548 non-native species in the central zone, a difference possibly associated with the geographic definition of this zone. This non-native flora contains a large number of families, none of which show any clear dominance, although the most common ones are Poaceae, Asteraceae and Fabaceae, in accordance with the three most invasive families worldwide (Pyšek, 1998). Most of Chile’s non-native species are annual plants (56%) of Eurasian- Mediterranean origin (68%). The dominance of exotic annual species coincides with the findings of other authors for other Mediterranean-climate regions (Le Floc’h 1991; D’Antonio and Vitousek, 1992; Cowling et al., 1996; Figueroa et al., 2004; Norton et al., 2007). Their rapid growth and high reproduction rates, and capacity to resist unfavourable periods in the form of seeds makes them more competitive in repeatedly disturbed open spaces, such as those created by fire, ploughing or grazing (Le Floc’h, 1991; Gómez-González et al., 2010). As for biogeographical origin, our results show that they are preferentially from the Mediterranean Basin or, in the broader sense, Eurasia, which would coincide with the findings of several authors for Chile and other Mediterranean-climate areas (Montenegro et al., 1991; Arroyo et al., 2000; Holmgrem et al., 2000; Figueroa et al., 2004; Castro et al., 2005). The annual character and Mediterranean origin predominating in non-native Chilean plants could be related to the different use history from that of the Mediterranean Basin. The pastures of the Mediterranean basin have been subjected to an intense grazing regime involving bovines and other domestic herbivores for over 6000 years of its evolutionary history (Perevolotsky and Seligman, 1998). This long history of coexistence with natural and anthropic disturbances has determined processes of co-evolution between plants and agriculture (Di Castri, 1981; Cowling et al., 1996; Perevolotsky and Seligman, 1998; Holmgren, 2002; Hayes and Holl, 2003; Kimball and Schiffman, 2003; Ricotta et al., 2009; HilleRisLambers et al., 2010), which have selected the plants presenting more competitive traits in a context of continuous grazing such as, for example, forms of growth, concentration of nutrients in tissues or position of growth meristems, among others (Adler et al., 2004; Díaz et al., 2007). On the contrary, PASTOS 2012. ISSN: 0210-1270 PASTOS, 42 (2), 137 - 160 151 Martín-Forés et al. Plant species colonization in Chilean espinales

Chile’s Mediterranean region underwent a drastic transformation since the colonisation only 500 years ago and its native flora might not have co-evolved with large herbivores in the last 10 000 years. This lack of adaptation to continuous grazing means that, with the introduction of livestock, native species are negatively affected, which favours the establishment of alien species (Milchunas and Lauenroth, 1993; Holmgren et al., 2000; Adler et al., 2004; Díaz et al., 2007). The flora of is a good expression of the country’s as a wholewith regard to percentages of the most represented families, life cycle and origin of non- native species. This central zone, representing only 20% of Chile’s territory, contains 80% of all the country’s exotic plants. This high concentration of naturalised plants (Matthei, 1995) can be accounted for by a conjunction of factors relating to history, environment and land uses. Chile was conquered by land from the north through the into the central zone. To the south of the Bío-Bío river, the territory was not colonised until just over a century ago (Aronson et al., 1998). Given the arid and semiarid conditions of the North, only the central zone, with its Mediterranean climate, was suitable for agriculture and for 350 years, the species introduced were therefore relegated to this region (Fuentes et al., 2008). It was only as from the XX century that non-native species were introduced into the whole country, with mass and intense deforestation of the austral temperate forest (Donoso and Lara, 1996). In short, it is the central zone that has undergone the biggest change as a result of intensive agriculture for over five centuries (Montenegro et al., 1991; Matthei, 1995). Moreover, it is the most densely populated region (78% of the country’s population, with an average of 75 inhabitants/km2; Pauchard et al., 2006; INE, 2007) and with the densest roads network (Arroyo et al., 2000). The representation of the non-native flora tends to be greater at more detailed spatial scales (Gaertner et al., 2009), a fact that can be seen in the espinales studied. On one hand, the percentage of non-native species therein is much higher than the 13% for the whole country or the 18% for the central zone, reaching 49%. This value is higher than the 36.8% reported by Figueroa et al. (2011) for espinales and very similar to that reported by Montenegro et al. (1991). At family level, the percentages of Caryophyllaceae, Rosaceae, Geraniaceae and Rubiaceae double and even quadruple the values characteristic of the country or of the central zone. On the other hand, among non-native species, annual plants show an increase from 56% for the whole country to 84%; exotic woody species were absent from our study. Finally, compared with the 68% of species of Eurasian or Mediterranean origin in Chile, the espinales account for 97%. In this context it is interesting to highlight the relationship between regions of origin and species’ biological cycle, with a positive association among annual plants for species from the Mediterranean Basin and among woody plants for those of Australian, African 152 PASTOS, 42 (2), 137 - 160 PASTOS 2012. ISSN: 0210-1270 Martín-Forés et al. Plant species colonization in Chilean espinales or American origin. This relationship is possibly associated with the way in which the species were introduced into the country and with the climatic characteristics of the recipient habitat: unintentionally in the case of most of the plants associated with agriculture and livestock farming (Mediterranean annual plants adapted to grazing; Holmgren, 2002) or for ornamental or forestry purposes (woody plants generally of extra-European origin; Pyšek et al., 2011). The extreme values found in the espinales (compared with the rest of Chile) referring to distribution of families, biogeographic origin and life cycle are, however, of the same order of magnitude as those found in Spanish grasslands (although proportionally Rubiaceae, Rosaceae and Geraniaceae present higher percentages in Chilean espinales and Brassicaceae in Spanish grasslands). Given that Europe, and specifically the Mediterranean Basin, have constituted the main source of immigration since America was discovered (Di Castri, 1991; Figueroa et al., 2004; Jiménez et al., 2008) the floristic similarity between both countries appears to indicate that the espinales represent a copy of Europe’s agricultural model, in which not only animal and plant species (livestock, cereals and associated weeds) were introduced from Europe, but also technology (ploughing, harrowing, animal traction) and the culture associated with management of the system (fallow, rotation). The final result is an agroecosystem, the Chilean espinal, which not only presents great physiognomic and functional similarity with the Spanish dehesa (Ovalle and Avendaño, 1987; Ovalle et al., 1990), but is also similar with regard to the floristic characteristics evaluated in this research. There are, however, differences between these two agroecosystems, particularly with regard to species richness (much higher in Spain). It is known that the number of alien species becoming established in a given country is lower than the amount that might potentially arrive (Malo and Suárez, 1997) and the number of exotic species capable of reaching Chile is estimated at between 7 070 and 35 400 (Castro et al., 2005). An example is the Santiago Botanic Garden which, in the middle of the XIX century, cultivated over 2000 exotic species, 43 of which became naturalised (Matthei, 1995; Castro et al., 2005). These data place in doubt whether the flora of the espinales constitutes an impoverished version of Spanish grasslands because specific filters existed that limited the number of species arriving or, on the contrary, whether there is a predominance of the biotic and abiotic filters acting in the assemblage of communities in the espinales. The entry of alien species and the extinction of native ones in a region have been considered a process of global biological homogenisation (McKinney and Lockwood, 2001; Olden, 2006; Olden and Rooney, 2006; Winter et al., 2009). Castro and Jaksic (2008) conclude that this homogenisation process is not yet significant in Chile, given that from colonisation times up to the present, only two species have become extinct (Plazia cheiranthifolia (Remy) Wedd. and Menodora linoides Phil.) and that the floristic similarity among regions has not significantly changed. Our data, however, and those PASTOS 2012. ISSN: 0210-1270 PASTOS, 42 (2), 137 - 160 153 Martín-Forés et al. Plant species colonization in Chilean espinales provided by Jiménez et al. (2008) and Figueroa et al. (2011), would seem to suggest that at least the espinales are being subjected to an intense homogenisation process, as can be seen in the dominance of certain species (and families) common to Spanish grasslands on the list of most frequent species in the espinales. The most frequent species is Leontodon taraxacoides (Vill.) Mérat, first recorded in Chile in 1963 (Castro et al., 2005), which contradicts the hypothesis that the exotic species appearing subsequent to 1950 present a narrower range within the country (Arroyo et al., 2000; Pauchard et al., 2004; Castro et al., 2005). This would appear to indicate that this homogenisation process has become accentuated in the last few decades. At present the speed of change of many ecological, economic and social parameters is reaching heretofore unknown rates, and the predictions are even more drastic in reference to changes in land uses at global scale (Lugo and González, 2010; USDA, 2006). In this context of global change, there is a pressing need to understand these processes of species colonisation and naturalisation. The exchange of species, successful establishment of some of them or extinction of others undoubtedly contributes to the appearance of new environmental scenarios, with socioeconomic repercussions that are difficult to evaluate in the short term (Rockstrom et al., 2009). Identifying changes in ecosystem structure and functioning in the short, medium and long term constitutes a fundamental objective with regard to evaluating the “health” of ecosystems, as is stated in the objectives of the Millennium Ecosystem Assessment Programme (Millennium Ecosystem Assessment, 2005; Carpenter et al., 2009).

ACKNOWLEDGMENTS

This research was supported by Spanish Ministry of Science and Innovation project CGL2009-08718. We are grateful to the Spanish Ministry of Education, Culture and Sport for providing a FPU PhD fellowship to I. Martín-Forés, the Government of Aragon for awarding a research fellowship to the Residencia de Estudiantes; and finally, to the Residencia de Estudiantes itself for its support.

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FLORA DE LA CUENCA MEDITERRÁNEA EN LOS ESPINALES CHILENOS: EVIDENCIAS DE UNA COLONIZACIÓN

RESUMEN

En la región mediterránea de Chile más del 18% de las especies de plantas son exóticas. Este hecho es especialmente importante en algunos sistemas agrosilvopastorales, como los espinales, muy similares funcionalmente a las dehesas españolas y de gran interés ecológico y socioeconómico. En este trabajo se analiza la flora no nativa de Chile considerando tres escalas de análisis: nacional, regional (zona central de clima mediterráneo) y a escala de comunidad (los espinales dentro de la región central), comparándola con la flora registrada en áreas equivalentes de la Península Ibérica. Se discuten los posibles mecanismos que han podido operar en la colonización florística desde la cuenca mediterránea hacia la región mediterránea chilena.

Palabras clave: Biogeografía, Chile, ciclo biológico, España, especies exóticas.